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Home , Centrostephanus, Echinus (sea urchin), Heliocidaris, Holothuria mexicana, Loxechinus albus, Lytechinus variegatus

International Conference on Agricultural, Ecological and Medical Sciences (AEMS-2014) July 3-4, 2014 London (United Kingdom)

Sea Urchins (Echinodermata: Echinoidea): Their Biology, Culture and Bioactive Compounds

M. Aminur Rahman*, A. Arshad, and Fatimah Md. Yusoff

 fishery is closely connected to that of the fisheries, whose fortune Abstract—The gonads of both male and female sea urchins, will eventually depend upon the stock enhancement, culture commonly known as " Roe”, are culinary delicacies in improvement, quality roe production and market forces that will many parts of the world. The roe of sea urchins is considered as a shape this rising industry in a very worthwhile and significant prized delicacy in Asian, Mediterranean and Western Hemisphere manner. countries and have long been using as luxury foods in Japan. Japanese demand for sea urchins raised concerns about overfishing, Keywords—Sea urchin, Biology, , Enhancement, thus making it one of the most valuable sea foods in the world. The Roe, Bioactive compounds. population of the Asian Pacific Region has been using it for long time as a remedy for improving general living tone and treatment for I. INTRODUCTION a number of diseases. Sea urchin gonads are also rich in valuable EA urchins are classic objects of research in different bioactive compounds, such as polyunsaturated fatty acids (PUFAs) S fields of biology, , biodiversity and evolution. At and β-carotene. PUFAs, especially eicosapentaenoic acid (EPA, the same time, they are used as raw material to produce C20:5) (n-3)) and docosahexaenoic acid (DHA C22:6 (n-3)), have foodstuff, in particular, the product of processing gonads significant preventive effects on arrhythmia, cardiovascular diseases known as "Sea urchin Roe" [1−3]. The roe of sea urchins is and cancer. β-Carotene and some xanthophylls have strong pro- vitamin A activity and can be used to prevent tumor development considered to be a prized delicacy due to its tasty qualities in and light sensitivity. Sea urchin fisheries have expanded so greatly Asian and Mediterranean countries, and also in Western in recent years that the natural population of sea urchins in Japan, Hemisphere countries such as Barbados and Chile [1, 4−6]. France, Chile, the northeastern United States, the Canadian The gonads of sea urchins either fresh or in the form of Maritime Provinces, and the west coast of North America from processed food have long been using as luxury foods in Japan California to British Colombia have been overfished to meet the [7]. Sea urchin is usually known as “uni” in Japan and its roe great demand. Not surprisingly, the decrease in supply and the can retail for as much as AU$450/kg [8]. It is served raw as continued strong demand have led to a great increase in interest in sashimi or in sushi, with soy sauce and wasabi. Japan imports aquaculture of sea urchins. Most, if not all, sea urchin fisheries have large quantities from the United States, South Korea and followed the same pattern of rapid expansion to an unsustainable peak, followed by an equally rapid decline. World landings of sea other producers. Japanese demand for sea urchin has raised urchin, having peaks at 120,000 mt in 1995, are now in the state of concerns about overfishing, thus making it one of the most about 82,000 mt. However, over half this catch comes from the valuable sea foods in the world [9]. The population of the recently expanded Chilean fishery for . In Europe, Asian Pacific Region has also been using it for long time as a the sea urchin stocks (Paracentrotus lividus) of first France and then remedy for improving general living tone, treatment for a Ireland were overfished in the 1980s to supply the French markets. number of diseases and strengthening of the sexual potency of These decreasing patterns clearly reflect the overexploitation of men, especially the middle aged [5, 10]. Sea urchin fisheries most fishery grounds and highlight the need for conservation have expanded so greatly in recent years that the natural policies, fishery management and aquaculture development. When population of sea urchins in Japan, France, Chile, the the wild stocks decline, high market demand for food, nutraceuticals and pharmaceuticals, raises the price of the product and, as a result, northeastern United States, the Canadian maritime provinces, culturing is most likely to become commercially viable. As this and the west coast of North America from California to review shows, there have been dramatic advances in the culture British Colombia have been overfished to meet the great methods of sea urchins in the last 15–20 years; we can conclude that demand [11−15]. Not surprisingly, the decrease in supply and currently the major obstacles to successful cultivation are indeed the continued strong demand have led to a great increase in managerial, cultural, conservational and financial rather than interest in aquaculture of sea urchins, particularly, in those biological and ecological. Therefore, the fate of the sea urchin areas where their populations have been depleted [4]. The sea urchin gonads that are of commercial importance can be M. Aminur Rahman*, Laboratory of Marine Biotechnology, Institute of obtained from a number of genera: Centrostephanus, Bioscience, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Diadema, Arbacia, Echinus, Loxechinus, Paracentrotus, Malaysia. A. Arshad, and Fatimah Md. Yusoff are with Laboratory of Marine , Anthocidaris, Colobocentrotus, Biotechnology, Institute of Bioscience, Universiti Putra Malaysia, 43400 UPM Echinometra, Evechinus, , Hemicentrotus, Serdang, Selangor, Malaysia and Department of Aquaculture, Faculty of Strongylocentrotus, , Pseudoboletia, Agriculture, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor, Malaysia Pseudocentrotus, Toxopneustes, and [16−19]. *Corresponding author's E-mail: [email protected] Most, if not all, sea urchin fisheries have followed the same

http://dx.doi.org/10.15242/IICBE.C714075 39 International Conference on Agricultural, Ecological and Medical Sciences (AEMS-2014) July 3-4, 2014 London (United Kingdom) pattern of rapid expansion to an unsustainable peak, followed substrates and is found at depths of 2 to 30 meters [19]. They by an equally rapid decline. World landings of sea urchin graze near the substrate, and their diet comprises , (Fig. 1), having peaks at 120,000 mt in 1995, are now in the periphyton, and sea grass. Growth is rapid and longevity low. state of about 82,000 mt with an alarming decreasing rate of A maximum size of 160 mm TD (test diameter) is reported, 32% [20, 21]. Nevertheless, over half amounts of this catch which corresponds to an age of four to five years. Individuals comes from the recently expanded sea urchin (Loxechinus can reach 75 mm TD in the first year. albus) fishery from Chile [22]. The other major sea urchin has an annual reproductive cycle mediated by seawater temperature, day length and feeding activity. Spawning fisheries, in terms of tonnage landed, are in Japan, Maine occurs during mid and later winter, when temperatures and (USA), British Colombia (Canada) and California (USA) day lengths are the lowest. [23]. In Europe, the sea urchin (Paracentrotus lividus) fishery of France and Ireland were overfished to supply the French Kina (Evechinus chloroticus) markets [24]. There are large populations of edible urchins in Kina is endemic to New Zealand where its distribution is Scotland ( and ) strongly associated with beds with individuals occurring and Norway (Strongylocentrotus droebachiensis), but these either within beds or aggregating in adjacent barrens. Kina is stocks are not suitable to commercial fishing as their roe usually found from the intertidal zone to 14 m but have been content is either very low or too variable [22, 25−27]. recorded from 60 m. It has a moderate growth rate with However the continuous decreasing patterns clearly reflect the individuals reaching 50 mm TD at 4 years of age. The overexploitation of most fishery grounds and highlight the maximum size of 80 to 100 mm TD is attained in 8 to 9 need for appropriate conservation strategies, fishery years. The mean longevity of individuals varies between sites management policies and aquaculture development but is between 10 to 20 years [28]. Kina attains sexual maturity at 40 to 50 mm TD (3 to 4 years of age) and initiatives. spawning occurs in spring.

Purple sea urchin (Heliocidaris erythrogramma) This sea urchin is distributed in the shallow coastal waters (intertidal to 35 m) of southern Australia. In Tasmania, it is common in kelp communities and in barrens, where it feeds by grazing and capturing drift weeds. On the Australian mainland, it can occur in high densities in association with sea grass beds [29]. Growth rates vary depending on nutrition but are generally moderate with individuals attaining 40 mm TD at one year and harvestable sizes (60 mm TD) at 3 to 5 years. Invalidated aging suggests that individuals can live for over 10 years and maximum sizes of 122 mm TD have been observed [30]. Sexual maturity is reached at 40–50 mm TD Fig. 1. Global sea urchin fisheries from 1950 to 2008 by fishing and 5 to 6 years of age [31]. Spawning occurs from summer [20]. to autumn with the best roe recoveries (10–14%) in August to December. II. SEA URCHIN BIOLOGY AND ECOLOGY The major sea urchin producing areas of the world are Erizo (Loxechinus albus) associated with major sites of primary productivity. In the The erizo or Chilean , Loxechinus albus, is temperate regions, these are usually associated with kelp a relatively slow-growing urchin found along the Pacific coast forests and in the subtropical and tropical regions, with sea of South America from Isla Lobos de Afuera in Peru to the grass beds. Given the similar habitat types, the various Southern tip of South America at depths ranging from of edible sea urchins share some similarities in intertidal to as deep as 340 m. [32]. These urchins can live to distribution and reproduction. However, they are varied in as old as 20 years and reach sizes up to TD 130 mm [23]. It is their basic biological characteristics, such as growth, maturity one of the most economically important species along the SW and longevity. coast of South America where it has been used as a food source since pre-Columbian times. These urchins have a Tripneustes gratilla strong preference for exposed habitats and are rare in This species (has a circumtropical distribution extending protected environments, apparently for reasons related to into the subtropics. It is found in the waters of the Indo- differential availability of larvae [32]. Its distribution is Pacific, Hawaii, and the Red Sea and is distributed from associated with kelp beds and it is most abundant below 40oS. Mozambique to the Red Sea, westward to Hawaii and Clarion The species is relatively slow growing, reaching a maximum Island, eastward to Paumotu, and as far south as Port Jackson. size of 130 mm TD and may live to 20 years. Spawning time It also occurs at Shark's Bay on the west coast of Australia. It varies along its distribution; occurring in spring to summer in is most common in very shallow water on a variety of hard

http://dx.doi.org/10.15242/IICBE.C714075 40 International Conference on Agricultural, Ecological and Medical Sciences (AEMS-2014) July 3-4, 2014 London (United Kingdom) the north, summer in the south and spring in the extreme Red sea urchin (Strongylocentrotus franciscanus) south. The red sea urchin Strongylocentrotus fransiscanus is the Lytechinus variegatus largest sea urchin in the world and is common along the West Coast of North America from Baha California to the Aleutian This species is distributed through the shallow waters of Archipelago and the coast of Siberia and north Asia. They the tropics to subtropics of the western Atlantic, from Florida, have been reported from as far south as the tip of Baja through the Caribbean to [33]. It is associated with sea California, Mexico (23oN) but their abundance declines at grass beds and hard bottoms covered with algae. Growth is sites south of the Vizcaino Peninsula (27oN). Their range rapid and longevity is limited. Individuals can reach 40 mm extend northwards up the west coast to Sitka and Kodiak AK TD at one year and a maximum size of 92 mm TD is reported at 58oN [37]. It is common in the subtidal zone to 50 m and is with a maximum age of 3 years. Mean longevity is between 1 strongly associated with kelp forests. Early growth is and 2 years. Sexual maturity is reached at 40 mm TD and relatively rapid and the species exhibits extreme longevity. there is no seasonality to spawning. Size at recruitment is around 90 mm TD which is reached in Common sea urchin (Paracentrotus lividus) around 6 to 8 years. The maximum size is around 200 mm This sea urchin is distributed through the shallow TD and individuals over 150 mm TD are older than 100 years (sublittoral to 20 m) waters of the Mediterranean and the [37]. Sexual maturity is attained at about 50 mm TD and north east Atlantic. It is strongly associated with sea grass spawning occurs over spring and summer. meadows and also occurs on encrusted rocky substrates where Strongylocentrotus intermedius it will form permanent burrows. Growth rates are moderate The Japanese green sea urchin, Strongylocentrotus with individuals of 40 mm TD being 4 to 5 years old and intermedius, is the second most commercially important individuals of 70+ mm being older than 12 years. A urchin in Japan. This species is distributed along the Asian maximum size of 75 mm TD is reported [34]. Individuals and Siberian coast of the Pacific. It is common in shallow mature at 13 to 20 mm TD and spawning occurs in spring to waters around Hokkaido and is harvested commercially in early summer. Irate, Aomori and Hokkaido [38]. It usually occurs on shallow Psammechinus miliaris rocky bottom and is associated with kelp [38]. It has small This species is restricted to the southern and eastern reddish-yellow gonads which have a nice sweet taste and is waters of the where it occurs from the littoral to listed on Tsukiji as Japanese. This species is adapted cold depths of 100 m. Its distribution is highly associated with the water though and the growth restriction does not appear to be kelp . Growth rates are moderate and longevity is a temperature related limit [38]. Growth varies depending on short. A maximum size of 45 mm TD is reported which density and nutrition. In high growth conditions, individuals corresponds with an age of between 3 to 4 years. Sexual reach 40 mm TD in 2 to 4 years and maximum sizes of over maturity is attained in the first year at 6 to 7 mm TD and 55 mm at ages of 6 to 10 years. Sexual maturity occurs at spawning occurs in summer. around 30 to 35 mm TD (2 years of age) and spawning occurs in spring and autumn. Green sea urchin (Strongylocentrotus droebachiensis) Strongylocentrotus nudus The green sea urchin has a circumpolar distribution, which provides for a very wide distribution through the North Strongylocentrotus nudus listed on Tsukiji as Japanese, is Atlantic (Scandinavian and North American coasts, Iceland the most commonly harvested edible sea urchin in Japan and and Greenland) to the North Pacific (North American and accounts for ~ 44% of the total commercial harvest [39]. It is Siberian coasts). Fisheries for S. droebachiensis are found on inter- and sub-tidal rocky bottoms extending from concentrated in Maine and the Canadian Maritimes but Dalian, China northwards to Primorskyi Kray, Russia and in smaller fisheries are prosecuted in Alaska, BC, Washington Japan where it is found in the Pacific from Sagami Bay to and Iceland. It is most common in the intertidal zone to 50 m Cape Erimo on Hokkaido and in the Sea of Japan from Omi where it is associated with [35]. Growth rates are Island in Yamaguchi to Soya Cape northern Hokkaido. The moderate and off Maine two distinct growth forms have been urchins generally reach the legal size (40 mm) in 2 to 4 years identified. A fast growing form reaches the minimum legal when feeding on perennial Laminarians whereas they may size at 4 to 6 years and may live for 16 to 20 years. The slow take 7 to 8 years on coralline flats. It occurs in the intertidal growing form lives for 8 to 12 years and never reaches the to subtidal rocky reefs and is strongly associated with kelp minimum legal size [23]. The minimum legal size in BC is communities. Juveniles recruit to coralline flats and move to 55 mm TD and the time required to grow to this size is adjacent kelp forests. In kelp forests individuals reach 50 mm thought to range between 4 and 8 years in most cases [36]. TD in 2 to 4 years, whilst this will take individuals 7 to 8 The maximum size is around 100 mm TD. Individuals reach years on coralline flats [39]. Maximum longevity is reported sexual maturity and first spawning at 45-50 mm TD. as 14 to 15 years. Sexual maturity is attained at 40 to 45 mm Spawning is generally occurring from mid-winter to early TD, and spawning takes place in autumn. spring.

http://dx.doi.org/10.15242/IICBE.C714075 41 International Conference on Agricultural, Ecological and Medical Sciences (AEMS-2014) July 3-4, 2014 London (United Kingdom)

Purple sea urchin (Strongylocentrotus purpuratus) III. SEA URCIN AQUACULTURE, MANAGEMENT AND The purple sea urchin is distributed along the Pacific coast ENHANCEMENT of North America and is abundant in the intertidal zone but A. Aquaculture has been recorded to 150 m [37]. It is strongly associated with kelp forest beds. Growth is highly variable and dependent on Generally, the edible sea urchins belong to the regular food availability. The maximum size is around 100 mm TD Echinoids [19], having separate sexes and are broadcast and age at first maturity is one or two years. spawners. During the breeding season, the matured individuals shed their gametes in seawater column where Purple crowned urchin (Centrostephanus rodgersii) fertilization occurs. The fertilized eggs develop to form This species has a subtropical distribution through waters pluteus larvae, which after a period of planktonic of eastern Australia and New Zealand. Recent reports of a development, feeding on microalgae, settle to a suitable southerly range extension into Bass Strait and the east coast substratum and undergo metamorphosis to form tiny juvenile of Tasmania [40] are probably associated with warming of sea urchins. Larval life cycle is almost around 1 month at 26- coastal waters, but this may be episodic [41]. It is associated 28°C, including the feeding or four-armed stage, the six to with hard in the north of its distribution and kelp eight-armed stages and settling competent stage (Fig. 2). The communities in the south, where it forms extensive barrens. Growth rates are moderate with individuals of 70 to 90 mm juveniles then grow on microalgae and the estimated time for TD being between 4 to 10 years old. The maximum size of these young urchins to reach marketable size (40–50 mm) is 120 mm TD corresponds with an age of up to 20 years old. commonly in the range of 1–3 years, but varying according to Sexual maturity is attained at 40 to 60 mm TD, and spawning species [22]. occurs in winter. White sea urchin (Salmacis sphaeroides) Salmacis sphaeroides, commonly known as short-spined white sea urchin, is one of the rare species of regular echinoids, although it can be found in the warm Indo-West Pacific from China to Solomon Islands and Australia [42, 43], and Singapore [44]. It has almost cloudy while test (5.0 to 8.0 cm diameter) with numerous short white spines (1.0 to 1.5 cm). Some may have white spines with maroon bands, others with all maroon spines, and yet others with green and maroon bands. It can be found in the warm temperate regions including Johor Straits, between Malaysia and Singapore [14, 15, 44]. This sea urchin can be occurred at depth range between 0 and 90 m, however it is also found in shallow waters, especially in amongst sea grass meadows, reef and in muddy sublitoral zone or washed ashore [43]. Fig. 2. Spawning, fertilization and a complete larval life-cycle of the white sea urchin () [47]. Salmacis sphaeroides gets their food from algae, bryzoans, and and frequently feeds on algae that grow Sea urchin culture has been accomplished on a large scale on the substrates. Spawning occurs throughout the year. in Japan for many decades. Millions of juvenile urchins are produced in their hatcheries, for release to managed areas of Echinometra seafloor on the intertidal areas. The nationally co-ordinated The various species of Echinometra have a circumtropical reseeding program has developed to the extent that over 66 distribution and occur in shallow water but have been million juveniles were released on the reefs within which, recorded to 20 m. They occur commonly in and around reefs over 80% were Strongylocentrotus intermedius [48]. The and found from central Japan in the north, to southeast contribution of released sea urchins to the overall catch has Australia in the south, and from Clarion Island off Mexico in been estimated to be between 62 and 80%. There are also the east, and to the Gulf of Suez in the west [12, 45]. They are much smaller-scale reseeding programs operating in South generally small bodied, with maximum sizes of 85 mm test Korea and on Luzon Island in the Philippines [23]. The diameter (TD) and may live 8 to 10 years. They form burrows researchers and farms in southern Ireland, have been and territories that are defended. The species is the most developing methods for sea urchin (Paracentrotus lividus) cultivation for over 20 years [49], and until relatively recently effective herbivore and in the absence of predators can occur in France [50]. Echinoculture (Psammechinus miliaris, E. in densities that exceed the primary production potential [46]. esculentus, P. lividus) has been conducted in Scotland since 1995 and there are also established research teams on the east coast of North America – Florida, Alabama, Maine, New Hampshire, New Brunswick and Newfoundland – working on

http://dx.doi.org/10.15242/IICBE.C714075 42 International Conference on Agricultural, Ecological and Medical Sciences (AEMS-2014) July 3-4, 2014 London (United Kingdom)

S. droebachiensis and Lytechinus variegatus; on the west Scotland and in British Columbia, Canada. coast of North America, including California and British Columbia (S. droebachiensis, S. franciscanus, S. purpuratus); in Chile (Loxechinus albus); Norway (S. droebachiensis); Israel (P. lividus); and in New Zealand (Evechinus chloroticus) [22]. Brood stocks of sea urchin are usually collected from the wild when they attain appropriate sexual maturity. Gametes from both female and male urchins are obtained by injecting 0.5 M KCl into the coelomic cavity. Eggs are collected by inverting female urchins over a glass beaker filled with Fig. 4. Juveniles of Salmacis sphaeroides: A) 1-day-old juvenile, B) 3-month-old juvenile [14]. filtered sea water (FSW), while sperms in the most concentrated form are pipetted off the genital pores [14, 45, Most culturists use a natural biofilm or a specially seeded 51, 52]. Fertilization is usually done at limited sperm substrate created from species isolated locally and concentration and the resulting embryos are reared. The grown on a PVC wave plate. Optimizing diets for the early fertilized eggs hatch in approximately 10–15 h, depending on juveniles and/or the replacement of diatom biofilms with the species, to develop to a ciliated blastula. When the larvae artificial diets is probably one of the most challenging areas attain feeding stage (four-armed pluteus), they are cultured in left to research. The variation in size and subsequent glass bottles on a rotating roller with a larval density of 1-2 variation in growth rates of post-larvae remain a bottleneck in individual/ml. Larvae are supplemented with a cultured the supply of hatchery-reared juveniles. Hatchery reared juveniles are robust enough to survive, transfer to sea cages or phytoplankton (Chaetoceros calcitrans, Isochrysis galbana) other grow-out systems from a small size (5-mm test at concentrations of 4000, 6,000 and 8,000 cells per ml of diameter) [53, 55]. At this point they are weaned onto other medium daily at four-, six- and eight-armed pluteus stages, diets, soft macroalgae or artificial diets, depending on the respectively, until attaining metamorphic competence within grow-out culture protocols. 1 month after fertilization (Fig. 3). For the large-scale culture In the indoor small-scale aquaria-rearing condition, 1-day- in Japan, partial water exchange systems [53] and continuous old juveniles are reared in small aquaria (25 x 20 x 10 cm) flow-through systems are used [9]. The costly aspect of larval with aerated filtered seawater, and pieces of dead coral with culture is the need for the simultaneous production of coralline red algae as food [12, 45, 51]. Seawater is partially microalgae as live feed. However, sea urchin (Lytechinus changed twice a month with freshly filtered sea water. This is variegatus) larvae have recently been proven to be suited for continued for up to three months, by which time the juveniles culture on artificial diets [54]. attain 9.0–10.0 mm in test diameter. The three-month-old juveniles (Fig. 5A) are then transferred to glass aquaria (46 x 30 x 30 cm) supplied with aerated seawater at the culture unit of the laboratory of Marine Biotechnology, Universiti Putra Malaysia. Stocking density is maintained at 20 juveniles in each replicate aquarium and the urchins are fed with red alga (Amphiroa fragilissima), brown alga (Sargassum polysystum) Fig. 3. Larval developmental stages of shrot-spined white sea and sea grass (Enhalus acoroides) All the juveniles were fed urchin (Salmacis sphaeroides: A) 4-arm pluteus, B) 6-arm pluteus, ad libitum and water in each cultured aquarium was C) 8-arm pluteus, D) Competent with complete rudiment completely changed at every 2−3 months. After the culture growth [14]. period of one year, the urchins attain sexual maturity (Fig. Settlement and metamorphosis are the most critical stages 5B) and the red alga-fed urchins performed the best over the in the development and culture of sea urchin larvae. High brown- and sea grass-fed urchins (Rahman unpublished data). survival is dependent on the larvae being competent to In contrast to the Japanese systems where hatchery-reared metamorphose and then responding to settlement cues. juveniles are mainly released to managed areas of seafloor [9, Induction of metamorphosis in small-scale culture has 22, 53], researchers in other countries have experimented recently been performed on coralline red algal extracts + with a wide range of grow-out systems for juvenile and adult Chaetoceros diatom (50:50) in petri dishes (9.0 x 3.0 cm) urchins, ranging from relocation from poor to good feeding containing FSW [14]. Majority of the competent larvae are grounds [56] to the ranching of urchins caged on the seafloor metamorphosed to young juvenile within 1 day post- [57]. Hatchery-reared juveniles have been grown in settlement (Fig. 4A). They were then cultured on coralline suspended culture (Kelly 2002, 2005) in closed recirculation algal stones in aerated aquaria for three months by which systems [50] and in dammed rock pools in southern Ireland. time they attained appropriate juvenile sizes (Fig. 4B) for A sea-cage cultivation system of stacking baskets suspended stocking in grow out culture system. Sea urchin juveniles from a ladder-like structure over which a work barge or raft have been produced on a commercial or semi-commercial can operate is being developed by Norwegian researchers scale by hatcheries in Japan, South Korea, Ireland, Norway,

http://dx.doi.org/10.15242/IICBE.C714075 43 International Conference on Agricultural, Ecological and Medical Sciences (AEMS-2014) July 3-4, 2014 London (United Kingdom)

[58]. The time taken for juveniles of most species to reach Development Law provide the basis for stock enhancement market size is in the order of 1–3 years [22]. [62]. The goal of this program is to “develop and improve coastal fishing grounds systematically by the construction of artificial reefs and the release of seedlings”. Enhancement can comprise a number of different activities including direct stock enhancement through seeding of hatchery-raised juveniles, habitat improvement or restoration, creation of artificial reefs, predator control, thinning and/or roe enhancement through supplemental feeding to increase the product recoveries etc. Re-seeding has been especially applied

Fig. 5. Juveniles and adults of cultured Salmacis sphaeroides: in Japan since the late 1980's. The numbers have been fairly A) Three-month-old juveniles for stocking in grow-out culture, stable since 1997 with about 70-85 million juveniles reared to B) Sexually matured adults after the culture period of one year in about 5-10 mm TD and released each year primarily in the captive aquaria-rearing condition. areas with the largest historical harvests. Strongylocentrotus B. Management intermedius accounts for about 85% of the urchins released by Systems that accelerate growth to market size while the Japanese in Hokkaido [23]. Predator removal is required producing a uniform size class would give an economic as excess by sea stars etc. has been implicated in advantage. One possible route to obtaining sustainable and the few cases where the re-seeding did not have any benefit environmentally friendly systems for urchin culture is to on the subsequent urchin production and and sea stars further examine their potential in integrated systems. They are removed from the grounds using baited traps prior to the have already been shown to thrive in polyculture with the release of the urchins to control mortality in the immediate Atlantic salmon [59] and to have a role in land-based period after release. Government has considerable integrated systems [60]. However, many species are true involvement in the management of coastal fisheries, , so the potential for their integration into systems particularly in the provision of subsidies for enhancement and where natural prey items, for example, mussels, are already infrastructure development as well as management produced should be explored. coordination. A couple of studies have looked at the Classical fisheries science was developed in consideration contribution of re-seeding or habitat enhancement to the of offshore, open access and industrial fishing situations and actual abundance of urchins in harvest areas in a sort of the resulting management systems are not well adapted, or round-about way at localized sites around Hokkaido and particularly robust, when applied to more complex spatial estimated that re-seeded urchins comprised 62%, 66% and structure of small scale, inshore fishery resources [61]. The 80% of the catch in 1994, 1995 and 1996 respectively [62]. social significance of small scale inshore fisheries is much In Japan, translocation of the urchins is used for a number greater, given the numbers of fishermen and other players of related reasons. In areas where kelp forest development is involved, than the sometimes more productive offshore held back by excessive urchin densities, urchins are fisheries, which generally involve larger enterprises, higher sometimes removed and replaced with adult kelps to permit capital investment and limited numbers of fishermen. As a rapid development of complex kelp forests [62]. The urchins result, much of the challenge in ensuring the sustainability of may then be placed into intensive sea ranching pens where shellfish fisheries lies in developing and applying appropriate they are fed ad libitum and prepared for harvest some months utilization, assessment and management models. The down the road. Experiments have shown that Green Sea management measures that explicitly acknowledge spatial Urchins (GSU) at densities up to 35 kg/m have recorded structure of fishery resources, and are therefore the most recovery increases from 6% to over 18% in 11 weeks on an suitable for these sorts of fisheries, include [61]: artificial diet [58], although further finishing for about 6 i. territorial property and use rights including lease, weeks on a natural kelp diet is still required to get an traditional tenure systems etc.; acceptable taste profile at this point. The sea urchin ii. harvest rotation coupled with pulse fishing and/or Evechinus chloroticus is widely distributed around New thinning; Zealand but attempts to establish a commercial fishery have, iii. reproductive refugia and Marine Protected Areas; like Norway, not succeeded because of the poor product iv. experimental management with spatial control, quality and low recoveries. Experiments with ponding over 2 contrasting treatments and replication; month periods have seen recoveries increase to near 20% and v. localized enhancement including habitat manipulation, produced other quality improvements that bode well for the seeding and predator control. future but further research is still needed to reach an economic breakeven. There are a number of aquaculture sites C. Enhancement around New Zealand which are currently considered marginal Overfishing and a decline in world production have for mussel farming which would be suitable for urchin prompted increasing in enhancement as a means of at least ponding or culture [63]. Multi-disciplinary approaches are maintaining production. It is most developed in Japan where therefore needed for stock enhancement and both scientific the 1974 Coastal Fishing Ground Improvement and and user group advisors should be involved [64]. One method

http://dx.doi.org/10.15242/IICBE.C714075 44 International Conference on Agricultural, Ecological and Medical Sciences (AEMS-2014) July 3-4, 2014 London (United Kingdom) of enhancement that apparently works very well with Green naphtoquinone pigments, spinochromes [70] as well as their Sea Urchins simply requires the presence of a salmon net pen. analogous compound echinochrome A, of which was showed The urchins can apparently settle out quite abundantly on bactericidal effect was reported by Service et al. [71]. The such structures and grow quite nicely by feeding on the phenolic hydroxyl groups in these molecules also suggested fouling organisms on the mesh. This has also provided some that they could participate in antioxidant activity as was good opportunities for Canadian fishermen in BC for some observed in other well-known antioxidant polyphenols such easy harvests. as tea catechins. The similar structured compounds are also The current market system used for the urchin trade found in the shells of sea urchins and thus suggesting that developed in tandem with the wild fishery but this will no they as well as echinochrome A would act as antioxidant doubt change dramatically once cultured product is available substances similar to other polyphenolic antioxidants in in substantial quantities. Cultured production is more tightly controlled than from the wild fishery so that, as with the edible plants [72]. While squaric acid ester-based cultured salmon, the consistent availability of an invariably methodology was used in a new synthesis of echinochrome A, high quality product throughout the year will have a a polyhydroxylated napthoquinone pigment commonly tremendous impact on the urchin markets throughout the isolated from sea urchin spines [73]. The Sea urchin gonads world. Traditional harvesters of sea urchins do not generally contain polyhydoxylated naphthoquinone, echinochrome A, know much about the potential of aquaculture [65] and will which is potential in antioxidant activity [74]. Sea urchin likely tend towards obstructing its development as opposed to gonads are also rich in valuable bioactive compounds, such as recognizing the available advantages and applying them to polyunsaturated fatty acids (PUFAs) and β-carotene [75]. their own benefit. This will be unfortunate because if the wild PUFAs, especially eicosapentaenoic acid (EPA, C20:5) (n-3)) and cultured urchin fisheries could be more closely and docosahexaenoic acid (DHA C22:6 (n-3)), have integrated, both would stand to benefit. For example, the significant preventive effects on arrhythmia, cardiovascular gonad size and quality are quite easy to manipulate and the diseases and cancer [76]. β-Carotene and some xanthophylls economic yield of the roe can be dramatically and fairly easily have strong pro-vitamin A activity and can be used to prevent increased. This knowledge is probably directly applicable to tumor development and light sensitivity [77]. The the wild fishery and could contribute to an increase in quality, composition of these valuable components, however, varies value and profitability. Already, fisheries and aquaculture are greatly among different urchin species and is influenced by blurring together with respect to product (gonad) their natural diet as well as physiological processes i.e. enhancement and re-seeding of juveniles is coming to the fore in a number of countries [65] reproductive stage [19, 78]. On the other hand, the high levels of AA and EPA recently detected in Diadema setosum IV. BIOACTIVE COMPOUNDS FROM SEA URCHINS and Salmacis sphaeroides supported the development of aquaculture of sea urchins [79], since PUFAs are important Alike many other , sea urchins have for human nutrition [19]. been considered as well as to be examined as a source of biologically active compounds with biomedical applications V. CONCLUSION [22]. However, the potential of echinoids as a source of biologically active products are largely unexplored [66]. The This paper has been produced as a background document marine environment is an exceptional reservoir of bioactive for a review of the World’s sea urchin fisheries. To summarize the views, reports and publications of other natural products, many of which exhibit structural and scientists/researchers, it is apparent that sea urchin fisheries chemical features not found in terrestrial natural products. have a poor record of sustainability, as evidenced by the The richness of diversity offers a great opportunity for the declines recorded in Japan, Maine, California and South discovery of new bioactive compounds. Modern technologies Korea among others, as well as by the ad hoc and/or have opened vast areas of research for the extraction of ineffective management in many sea urchin fisheries. Very biomedical compounds from and seas to treat the few stocks have been formally assessed, meaning it is near deadly diseases. The number of natural products isolated from impossible to qualify declines as the -down of marine organisms increases rapidly, and now exceeds with accumulated biomass, which does not arrest the productivity hundreds of new compounds being discovered every year of the stock, or as a case of over-fishing in which case its [67]. The secondary metabolites have various functions; it is productivity may be forced into permanent decline. Small- likely that some of them may be pharmacologically active on scale management is mentioned time and again as offering humans and useful as medicines [68]. A majority of the most promise for ensuring long term sustainability. The pharmacologically active secondary metabolites have been strong and consistent spatial structure inherent in sea urchin isolated from [69]. There are much valuable stocks combined with excessive effort from mobile fleets and information for new antibiotic discoveries and give new inappropriately large scale, and therefore ineffective insights into bioactive compounds in sea urchin. The sea management all contribute to declining production in many of urchin shells are containing various polyhydroxylated the world’s sea urchin fisheries. This is particularly the case for the world’s largest sea urchins fishery in Chile where the

http://dx.doi.org/10.15242/IICBE.C714075 45 International Conference on Agricultural, Ecological and Medical Sciences (AEMS-2014) July 3-4, 2014 London (United Kingdom) risks of collapse cannot be discounted. Given that this fishery http://dx.doi.org/10.1111/j.1749-7345.1997.tb00966.x [5] Yur’eva, M.I., Lisakovskaya, O.V., Akulin, V.N., Kropotov, A.V. 2003. alone contributes upwards of 55% of the global harvest, a Gonads of sea urchins as the source of medication stimulating sexual significant decline in Chile’s fishery would likely lead to behavior. Russian Journal of Marine Biology, 29: 189–193. structural realignment in the market and higher prices for http://dx.doi.org/10.1023/A:1024681002304 [6] Rahman, M.A. and Yusoff, F.M. 2010. Sea urchins in Malaysian coastal mid-range products until aquaculture production ramped up. waters. The Oceanographer, 4(1): 20–21. There is also general agreement that some form of exclusive [7] Shimabukuro, S. 1991. Tripneustes gratilla (sea urchin). In: Shokita, S., access as a prerequisite condition to promote meaningful Kakazu, K., Tomomi, A., Toma, T., Yamaguchi, M. (Eds.). Aquaculture enhancement and intelligent harvesting to maximize roe in Tropical Areas. Midori Shobo Co. Ltd. Tokyo, pp. 313–328. [8] Richard, M. 2004. The little urchins that can command a princely price. value will provide the best hedge against uncertainties in The Sydney Morning Herald. fisheries productivity and market stability. In the short term it [9] Hagen, N.T., 1996. Echinoculture: from fishery enhancement to closed- is likely that global production of sea urchin roe from wild cycle cultivation. World Aquaculture, 27: 6–19. [10] Seifullah, R.D., Ankudinova, I.A. and Kim, E.K. 1995. Seksual’noe fisheries will decline, with the major production being provedenie muzhchin (sexual behavior of men). Izd. Yaguar, Moscow. provided by those fisheries that have supported active [11] Lawrence, J.M., Lawrence, A.L., McBride, S.C., George, S.B., Watts, S.A. management strategies to readjust effort and contain catches and Plank, L.R. 2001. Developments in the use of prepared feeds in sea- urchin aquaculture. World Aquaculture, 32(3): 34–39. to levels that provide long-term sustainability. Given that [12] Rahman, M.A., Uehara, T. and Lawrence, J.M. 2005. Growth and demand is unlikely to decline; future production will be heterosis of hybrids of two closely related species of Pacific sea urchins increasingly valuable. In order to make sea urchins fisheries ( Echinometra) in Okinawa. Aquaculture, 245: 121–133. viable and profitable, the following actions are suggested: http://dx.doi.org/10.1016/j.aquaculture.2004.11.049 [13] Rahman, M.A., Amin, S.M.N., Yusoff, F.M., Arshad, A., Kuppan, P. and  Refinement of artificial diet formulations for juveniles Shamsudin, M.N. 2012a. Length weight relationships and fecundity and adults to maximize growth rates and survivorship estimates of long-spined sea urchin, Diadema setosum, from the Pulau Pangkor, Peninsular Malaysia. Aquatic Ecosystem Health and and produce gonads of the desired taste, texture, flavor Management, 15: 311–315. and color. [14] Rahman, M.A., Yusoff, F.M., Arshad, A., Shamsudin, M.N. and Amin,  Optimization of grow-out facilities for juveniles and S.M.N. 2012b. Embryonic, larval, and early juvenile development of the tropical sea urchin, Salmacis sphaeroides (Echinodermata: Echinoidea). adults either at sea (in containers or ‘ranched’) or land The Scientific World Journal, 2012: 1–9. based; http://dx.doi.org/10.1100/2012/938482  Regulations regarding fishing methods, fishing areas and [15] Rahman, M.A., Arshad, A., Yusoff, F.M. and Amin, S.M.N. 2013. Hybridization and growth of tropical sea urchins. Asian Journal of protection of company investments need to be developed. and Veterinary Advances, 8(2): 177–193.  Better surveillance of sea urchin density to guarantee a http://dx.doi.org/10.3923/ajava.2013.177.193 steady flow of raw materials. [16] Sloan, N.A. 1985. fisheries of the world: a review. In: Keegan, B.F. and O' Connor, B.D.S. (Eds.), Echinoderms. A.A. Bolkema,  Areas need to be thinned out to get the best possible Rotterdam, pp. 109–124. product for the market, this is also necessary for the kelp [17] Saito, K. 1992. Sea urchin fishery of Japan. In: Anonymous, The forest to grow back. management and enhancement of sea urchins and other kelp bed resources: a Pacific rim perspective. California Sea Grant College, La Jolla. Rep. No.  More capital needs to be directed towards investing in T-CSGCP-028. technology for processing to reduce labor costs and [18] Keesing, J.K., Hall, K.C. 1998. Review of the status of world sea urchin preserve product quality. fisheries points to opportunities for aquaculture. Journal of Shellfish  Improved cooperation between fishermen and processors, Research, 17(5):1597–1604. [19] Lawrence, J.M. 2007. Edible Sea Urchins: Biology and Ecology. Elsevier, when marketing and selling the sea urchins. Boston, 380 p. [20] FAO. 2010. The State of World Fisheries and Aquaculture 2010. Food and ACKNOWLEDGMENT Agriculture Organization of the United Nations, Rome, Italy. [21] Carboni, C., Addis, P., Cau, A. and Atach, T. 2012. Aquaculture could We would like to express our grateful thanks and enhance Mediterranean sea urchin fishery, expand supply. Global appreciations to the Universiti Putra Malaysia (UPM) for Aquaculture Advocate, 44–45. providing financial supports through Research Management [22] Kelly, M.S. 2005. Echinoderms: their culture and bioactive compounds. In: Matranga, V. (Ed.), Echinodermata: Progress in Molecular and Subcellular Centre (RMC) under Research Universiti Grant Scheme Biology. Subseries: Marine Molecular Biotechnology. Springer-Verlag, (RUGS) vide Project No. 05-02-12-2184RU. Berlin Heidelberg, pp. 139–165. [23] Andrew, N.L. et al. 2002. Status and management of world sea urchin REFERENCES fisheries. Oceanography and Marine Biology, An Annual Review, 40: 343–425. [1] Kaneniwa, M. and Takagi, T. 1986. Fatty acids in the lipid of food [24] Barnes, D.K.A., Verling, E., Crook, A., Davidson, I, and O’Mahoney, M. products from sea urchin. Bulletin of the Japanese Society of Scientific 2002. Local population disappearance follows (20 yr after) cycle collapse Fisheries, 52(9): 1681–1685. in a pivotal ecological species. Marine Ecology Progress Series, 226: 311– http://dx.doi.org/10.2331/suisan.52.1681 313. [2] Oshima, T., Wada, S. and Koizumi, C. 1986. Lipid deterioration of salted http://dx.doi.org/10.3354/meps226311 gonads of sea urchin during storage at 5oC. Bulletin of the Japanese [25] Hagen, N.T. 2000. Echinoderm culture. In: Stickney, R.R. (Ed.), Society of Scientific Fisheries, 52(3): 511–517. Encyclopedia of aquaculture. Wiley-Interscience, New York, pp. 247–253. http://dx.doi.org/10.2331/suisan.52.511 [26] Kelly, M.S. 2000. The reproductive cycle of the sea urchin Psammechinus [3] Ichihiro, K. 1986. Breeding, processing and sale, Hokkai Suisan miliaris (Gmelin) (Echinodermata: Echinoidea) in a Scottish sea loch. Shinbunsha, Sappro, Japan. Journal of the Marine Biological Association of the United Kingdom, 80: [4] Lawrence, J.M., Olave, S., Otaiza, R., Lawrence, A.L. and Bustos, E. 909–919. 1997. Enhancement of gonad production in the Sea Urchin Loxechinus http://dx.doi.org/10.1017/S0025315400002897 albus in Chile fed extruded feeds. Journal of the World Aquaculture [27] Sivertsen, K. 2004. Harvestable sea urchin Strongylocentrotus Society, 28(1): 91–96. droebachiensis resources along the Norwegian coast. In: Lawrence, J.M.

http://dx.doi.org/10.15242/IICBE.C714075 46 International Conference on Agricultural, Ecological and Medical Sciences (AEMS-2014) July 3-4, 2014 London (United Kingdom)

and Guzman, O. (Eds.), Sea Urchins: Fisheries and Aquaculture. DEStech in the eastern Caribbean. FAO Fisheries and Aquaculture Circular No. Publications, Lancaster, Pennsylvania, pp. 85. 1056, FAO. 2010, Rome, Italy, 43p. [28] Barker, M.F. 2001. The ecology of Evechinus chloroticus. In: Lawrence, [48] Agatsuma, Y., Sakai, Y. and Andrew, N.L. 2004. Enhancement of Japan’s J.M. (Ed.), Edible Sea Urchins: Biology and Ecology, Elsevier, sea urchin fisheries. In: Lawrence, J.M. and Guzman, O. (Eds.), Sea Amsterdam, The Netherlands, pp. 245–260. urchins: fisheries and aquaculture. DEStech Publications, Lancaster, http://dx.doi.org/10.1016/S0167-9309(01)80016-8 Pennsylvania, pp. 18–36. [29] Kessing, J. 2001. The ecology of Heliocidaris erythrogramma. In: [49] Leighton, P. 1995. Contributions towards the development of Lawrence, J.M. (Ed.), Edible Sea Urchins: Biology and Ecology, Elsevier, echinoculture in North Atlantic waters with particular reference to Amsterdam, The Netherlands, pp. 261–270. Paracentrotus lividus (Lamarck). Ph.D. thesis, National University of http://dx.doi.org/10.1016/S0167-9309(01)80017-X Ireland, Galway. [30] Sanderson, C.J. 1995. Interim Sea Urchin Report February 1995 [50] Grosjean, P., Spirlet, C. and Gosselin, P. 1998. Land-based, closed-cycle Department of Primary Industry and Fisheries Marine Research Laboratory echinoculture of Paracentrotus lividus (Lamarck) (Echinoidea: International Report 21. Echinodermata): a long-term experiment at a pilot scale. Journal of [31] Sanderson, C.J., Le Rossignol, M. and James, W. 1996. A pilot program to Shellfish Research, 17(5):1523–1531. maximize Tasmania’s sea urchin (Heliocidaris erythrogramma) resource. [51] Rahman, M.A., Uehara, T. and Pearse, J.S. 2001. Hybrids of two closely Fisheries Research and Development Corporation Final Report 93/221. related tropical sea urchins (genus Echinometra): evidence against [32] Vasquez, J. 2001. The ecology of Loxechinus albus. In: Lawrence, J.M. postzygotic isolating mechanisms. Biological Bulletin, 200: 97–106. (Ed.), Edible Sea Urchins: Biology and Ecology Elsevier, Amsterdam, The http://dx.doi.org/10.2307/1543303 Netherlands, pp. 161–175. [52] Rahman, M.A., Uehara, T., Pearse, J.S., 2004. Experimental hybridization http://dx.doi.org/10.1016/S0167-9309(01)80012-0 between two recently diverged species of tropical sea urchins, Echinometra [33] Watts, S.A., McClintock, J.B. and Lawrence, J.M. 2001. The ecology of mathaei and Echinometra oblonga. Invertebrate Reproduction and Lytechinus variegatus. In: Lawrence, J.M. (Ed.), Edible Sea Urchins: Development, 45: 1– 14. Biology and Ecology. Elsevier, Amsterdam, The Netherlands, pp. 375– http://dx.doi.org/10.1080/07924259.2004.9652569 394. [53] Sakai, Y., Tajima, K.I. and Agatsuma, Y. 2004. Mass production of seed http://dx.doi.org/10.1016/S0167-9309(01)80023-5 of the Japanese edible sea urchins Strongylocentrotus droebachiensis and [34] Boudouresque, C.-F. and Verlaque, M. 2001. The ecology of Strongylocentrotus nudus. In: Lawrence, J.M. and Guzman, O. (Eds.), Paracentrotus lividus. In: Lawrence, J.M. (Eds.), Edible Sea Urchins: Sea urchins: fisheries and aquaculture. DEStech Publications, Lancaster, Biology and Ecology. Elsevier, Amsterdam, The Netherlands, pp. 177– Pennsylvania, pp. 287–298. 216. [54] George, S.B., Lawrence, J.M. and Lawrence, A.L. 2004. Complete larval http://dx.doi.org/10.1016/S0167-9309(01)80013-2 development of the sea urchin Lytechinus variegatus fed an artificial feed. [35] Scheibling, R.E. and Hatcher, B.G. 2001. The ecology of Aquaculture, 242(1-4): 217-228. Strongylocentrotus droebachiensis. In: Lawrence, J.M. (Ed.), Edible Sea http://dx.doi.org/10.1016/j.aquaculture.2004.06.024 Urchins: Biology and Ecology. Elsevier, Amsterdam, The Netherlands, pp. [55] Kelly, M.S. 2002. Survivorship and growth rates of hatchery-reared sea 271–297. urchins. Aquaculture International, 10: 309–316. http://dx.doi.org/10.1016/S0167-9309(01)80018-1 http://dx.doi.org/10.1023/A:1022414516929 [36] Taylor, P.H. 2004. Green Gold: Scientific findings for management of [56] Moylan, E. 1997. Gonad conditioning and wild stock enhancement of the Maine’s Green Sea Urchin fishery. Maine Department of Marine purple sea urchin Paracentrotus lividus on the west coasts of Ireland. Resources, Boothbay Harbour, Maine, USA. Bulletin of the Aquaculture Association of Canada, 97(1): 38–45. [37] Tegner, M. 2001. The ecology of Strongylocentrotus fransiscanus and [57] Cuthbert, F.M., Hooper, R.G. and McKeever T. 1995. Sea urchin Strongylocentrotus purpuratus. In: Lawrence, J.M. (Ed.), Edible Sea aquaculture phase I: sea urchin feeding and ranching experiments. Report Urchins: Biology and Ecology. Elsevier, Amsterdam, The Netherlands, pp. of Project AUI-503. Canadian Centre for Fisheries Innovation, 307–331. Government of Newfoundland. http://dx.doi.org/10.1016/S0167-9309(01)80019-3 [58] Aas, K. 2004. Technology for sea-based farming of sea urchins. In: [38] Agatsuma, Y. 2001a. The ecology of Strongylocentrotus intermedius. In: Lawrence J.M. and Guzmán O. (Eds.), Sea Urchins: Fisheries and Ecology, Lawrence, J.M. (Ed.), Edible Sea Urchins: Biology and Ecology. Elsevier, DEStech Publications, Inc., Lancaster, pp. 366–373. Amsterdam, The Netherlands, pp. 333–346. [59] Kelly, M.S., Brodie, C.C. and McKenzie, J.D. 1998. Somatic and gonadal http://dx.doi.org/10.1016/S0167-9309(01)80021-1 growth of the sea urchin Psammechinus miliaris (Gmelin) maintained in [39] Agatsuma, Y. 2001b. The ecology of Strongylocentrotus nudus. In: polyculture with the Atlantic salmon. Journal of Shellfish Research, 17(5): Lawrence, J.M. (Ed.), Edible Sea Urchins: Biology and Ecology. Elsevier, 1557–1562. Amsterdam, The Netherlands, pp. 347–361. [60] Shpigel, M., McBride, S.C., Marciano, S. and Lupatsch, I. 2004. http://dx.doi.org/10.1016/S0167-9309(01)80021-1 Propagation of the European sea urchin Paracentrotus lividus in Israel. In: [40] Edgar, G. 1999. Tasmania. In: Andrew, N.L. (Ed.), Under Southern Seas: Lawrence, J.M. and Guzman O. (Eds.), Sea urchins: fisheries and The Ecology of Australia’s Rocky Reefs, University of NSW Press, aquaculture. DEStech, Publications, Lancaster, Pennsylvania, 85 pp. Sydney. [61] Orensanz, J.M. and Jamieson, G.S. 1998. The assessment and management [41] Andrew, N. and Byrne, M. 2001. The ecology of Centrostephanus of spatially structured stocks: an overview of the North Pacific Symposium rodgersii. In: J.M. Lawrence (Ed.), Edible Sea Urchins: Biology and on Invertebrate Stock Assessment and Management. In: Jamieson, G.S. Ecology. Elsevier, Amsterdam, The Netherlands, pp. 149–160. and Campbell A. (Eds.), Proceedings of the North Pacific Symposium on http://dx.doi.org/10.1016/S0167-9309(01)80011-9 Invertebrate Stock Assessment and management. Edited by. Can. Spec. [42] Miskelly, A. 2002. Sea Urchins of and Indo-Pacific, Capricornica Publ. Fish. Aquat. Sci 125. pp. 441- 445. Publications, Sydney, Australia. [62] Agatsuma, Y., Sakai, Y. and Andrew, N.L. 2004. Enhancement of Japan’s [43] Schoppe, S. 2000. A guide to common shallow water sea stars, sea urchins, sea urchin fisheries. In: Lawrence, J.M. and Guzman, O. (Eds.), Sea sea cucumbers and feather stars (Echinoderms) of the Philippines. Times urchins: fisheries and aquaculture. DEStech Publications, Lancaster, Editions, Singapore, 144 p. Pennsylvania, pp. 18–36 [44] Tan, L.W.H. and Ng, P. K. L. 1988. A Guide to Seashore Life. Singapore [63] Barker, M.F. and Fell, J. 2004. Sea cage experiments on roe enhancement Science Centre, Singapore, 160 p. of New Zealand sea urchin Evachinus chloroticus. In: Lawrence, J.M. and [45] Rahman, M.A., Uehara, T. and Aslan, L.M. 2000. Comparative viability Guzmán, O. (Eds.), Sea Urchins: Fisheries and Ecology, DEStech and growth of hybrids between two sympatric species of sea urchins (genus Publications, Inc., Lancaster, Pp. 375–383. Echinometra) in Okinawa. Aquaculture, 183: 45–56. [64] Masuda, R. and Tsukamoto, K. 1998. Stock enhancement in Japan: http://dx.doi.org/10.1016/S0044-8486(99)00283-5 Review and perspective. Bulletin of Marine Science, 62(2): 337–358. [46] McClanahan, T.R. and Muthiga, N.A. 2001. The ecology of Echinometra. [65] Robinson, S.M. 2004. The evolving role of aquaculture in the global In: Lawrence, J.M. (Ed.), Edible Sea Urchins: Biology and Ecology. production of sea urchins. In: Sea Urchins: Fisheries and Ecology Elsevier, Amsterdam, The Netherlands, pp. 225–243. proceedings of the international Conference on Sea-Urchin Fisheries and http://dx.doi.org/10.1016/S0167-9309(01)80015-6 Aquaculture. Puerto Varas, Chile, March 25-27, 2003. DEStech [47] Pena, M.H., Oxenford, H.A., Parker, C. and Johnson, A. 2010. Biology Publications. Lancaster, PA. and fishery management of the white sea urchin, Tripneustes ventricosus,

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[66] Bragadeeswaran, S., Sri Kumaran, N., Prasath Sankar P. and Prabahar, R. 2013. Bioactive potential of sea urchin Temnopleurus toreumaticus from Devanampattinam, Southeast coast of India. Journal of Pharmacy and Alternative Medicine, 2(3): 9–17. [67] Proksch, P. and Muller, W.E.G. 2006. Frontiers in Marine Biotechnology. Horizon Bioscience: Norfolk, UK. [68] Briskin, D. 2000. Medicinal Plants and Phyto medicines. Linking plant biochemistry and physiology to human health. Plant Physiology, 124: 507–514 http://dx.doi.org/10.1104/pp.124.2.507 [69] Carballeria, N.M., Cruz, C. and A. Sostre. 1996. Identification of the novel 7-methyl-6 octadecenoic acid in mexicana. Journal of Natural Products, 59(11): 1076-1078. http://dx.doi.org/10.1021/np9605091 [70] Anderson, A.H., Mathieson, J.W. and Thomson, R.H. 1969. Distribution of spinochrome pigments in echinoids. Comparative Biochemistry and Physiology, 28: 333–345. http://dx.doi.org/10.1016/0010-406X(69)91347-4 [71] Service, M. and Wardlaw, A.C. 1984. Echinochrome-A as a bactericidal substance in the coelomic fluid of Echinus esculentus. Comparative Biochemistry and Physiology Part B, 79: 161–165. http://dx.doi.org/10.1016/0305-0491(84)90008-7 [72] Chantaro, P., Devahastin, S. and Chiewchan, N. 2008. Production of antioxidant high dietary fiber powder from carrot peels. LWT-Food Science and Technology, 41: 1987–1994. http://dx.doi.org/10.1016/j.lwt.2007.11.013 [73] Pena-Cabrera, E. and Liebeskind, L.S. 2002. Squaric acid ester-based total synthesis of Echinochrome A. Journal of Organic Chemistry, 67: 1689– 1691. http://dx.doi.org/10.1021/jo016034m [74] Lebedev, A.V., Levitskaya, E.L., Tikhonova, E.V. and Ivanova, M.V. 2001. Antioxidant properties, autoxidation and mutagenic activity of echinochrome A compared with its etherified derivative. Biochemistry, 66: 885–893. [75] Dincer, T. and Cakli, S. 2007. Chemical composition and biometrical measurements of the Turkish Sea urchin (Paracentrotus lividus, Lamarck, 1816). Critical Reviews in Food Science and Nutrition, 47(1): 21–26. http://dx.doi.org/10.1080/10408390600550265 [76] Pulz, O. and Gross, W. 2004. Valuable products from biotechnology of microalgae. Applied Microbiology and Biotechnology, 65(6): 635–648. http://dx.doi.org/10.1007/s00253-004-1647-x [77] Britton, G., Liaaen-Jensen, S. and Pfander, H. 2004. Carotenoids handbook. Birkhauser Verlag Boston, USA: http://dx.doi.org/10.1007/978-3-0348-7836-4 [78] Fernandez, C. 1998. Seasonal changes in the biochemical composition of the edible sea urchin Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment. Marine Ecology, 19: 1–11. http://dx.doi.org/10.1111/j.1439-0485.1998.tb00449.x [79] Chen, G. -Q., Xian, W. -Z., Lau, C. -C., Peng, J., Qiu, J. –W., Chen, F. and Jiang, Y. 2010. A comparative analysis of lipid and carotenoid composition of the gonads of Anthocidaris crassispina, Diadema setosum and Salinacis sphaeroides. Food Chemistry, 120(4): 973–977. http://dx.doi.org/10.1016/j.foodchem.2009.11.034

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